Visual Nonclassical Receptive Field Effects Emerge from Sparse Coding in a Dynamical System

Extensive electrophysiology studies have shown that many V1 simple cells have nonlinear response properties to stimuli within their classical receptive field (CRF) and receive contextual influence from stimuli outside the CRF modulating the cell's response. Models seeking to explain these non-classical receptive field (nCRF) effects in terms of circuit mechanisms, input-output descriptions, or individual visual tasks provide limited insight into the functional significance of these response properties, because they do not connect the full range of nCRF effects to optimal sensory coding strategies. The (population) sparse coding hypothesis conjectures an optimal sensory coding approach where a neural population uses as few active units as possible to represent a stimulus. We demonstrate that a wide variety of nCRF effects are emergent properties of a single sparse coding model implemented in a neurally plausible network structure (requiring no parameter tuning to produce different effects). Specifically, we replicate a wide variety of nCRF electrophysiology experiments (e.g., end-stopping, surround suppression, contrast invariance of orientation tuning, cross-orientation suppression, etc.) on a dynamical system implementing sparse coding, showing that this model produces individual units that reproduce the canonical nCRF effects. Furthermore, when the population diversity of an nCRF effect has also been reported in the literature, we show that this model produces many of the same population characteristics. These results show that the sparse coding hypothesis, when coupled with a biophysically plausible implementation, can provide a unified high-level functional interpretation to many response properties that have generally been viewed through distinct mechanistic or phenomenological models.Author Summary: Simple cells in the primary visual cortex (V1) demonstrate many response properties that are either nonlinear or involve response modulations (i.e., stimuli that do not cause a response in isolation alter the cell's response to other stimuli). These non-classical receptive field (nCRF) effects are generally modeled individually and their collective role in biological vision is not well understood. Previous work has shown that classical receptive field (CRF) properties of V1 cells (i.e., the spatial structure of the visual field responsive to stimuli) could be explained by the sparse coding hypothesis, which is an optimal coding model that conjectures a neural population should use the fewest number of cells simultaneously to represent each stimulus. In this paper, we have performed extensive simulated physiology experiments to show that many nCRF response properties are simply emergent effects of a dynamical system implementing this same sparse coding model. These results suggest that rather than representing disparate information processing operations themselves, these nCRF effects could be consequences of an optimal sensory coding strategy that attempts to represent each stimulus most efficiently. This interpretation provides a potentially unifying high-level functional interpretation to many response properties that have generally been viewed through distinct models.